Leafflower plant/leafflower moth brood pollination mutualisms are widespread in the Paleotropics. Leafflower moths pollinate leafflower plants, but their larvae consume a subset of the hosts’ seeds. These interactions are highly phylogenetically constrained: six clades of leafflower plants are each associated with a unique clade of leafflower moths (Epicephala). Here, we report a previously unrecognized basal seventh pollinating Epicephala lineage—associated with the highly derived leafflower clade Glochidion—in Asia. Epicephala lanceolaria is a pollinator and seed predator of Glochidion lanceolarium. Phylogenetic inference indicates that the ancestor of E. lanceolaria most likely shifted onto the ancestor of G. lanceolarium and displaced the ancestral allospecific Epicephala pollinator in at least some host populations. The unusual and apparently coadapted aspects of the G. lanceolarium/E. lanceolaria reproductive cycles suggest that plant-pollinator coevolution may have played a role in this displacement and provide insights into the dynamics of host shifts and trait coevolution in this specialized mutualism.